RINGTAILED LEMUR BIOLOGY Lemur Catta in Madagascar

RINGTAILED LEMUR BIOLOGY

Lemur Catta in Madagascar DEVELOPMENTS IN PRIMATOLOGY: PROGRESS AND PROSPECTS

Series Editor: Russell H. Tuttle University of Chicago, Chicago, Illinois

This peer-reviewed book series melds the facts of organic diversity with the continuity of the evolutionary process. The volumes in this series exemplify the diversity of theoretical perspectives and methodological approaches currently employed by primatologists and physical anthropologists. Specific coverage includes: primate behavior in natural habitats and captive settings primate ecology and conservation; functional morphology and developmental biology of primates primate systematics genetic and phenotypic differences among living primates and paleoprimatology.

COMPARATIVE VERTEBRATE COGNITION Edited by Lesley J. Rogers and Gisela Kaplan ANTHROPOID ORIGINS: NEW VISIONS Edited by Callum F. Ross and Richard F. Kay MODERN MORPHOMETRICS IN PHYSICAL ANTHROPOLOGY Edited by Dennis E. Slice BEHAVIORAL FLEXIBILITY IN PRIMATES: CAUSES AND CONSEQUENCES By Clara B. Jones NURSERY REARING OF NONHUMAN PRIMATES IN THE 21ST CENTURY Edited by Gene P. Sackett, Gerald C. Ruppenthal and Kate Elias NEW PERSPECTIVES IN THE STUDY OF MESOAMERICAN PRIMATES: DISTRIBUTION, ECOLOGY, BEHAVIOR, AND CONSERVATION Edited by Paul Garber, Alejandro Estrada, Mary Pavelka and LeAndra Luecke HUMAN ORIGINS AND ENVIRONMENTAL BACKGROUNDS Edited by Hidemi Ishida, Martin Pickford, Naomichi Ogihara and Masato Nakatsukasa PRIMATE BIOGEOGRAPHY Edited by Shawn M. Lehman and John Fleagle REPRODUCTION AND FITNESS IN BABOONS: BEHAVIORAL, ECOLOGICAL, AND LIFE HISTORY PERSPECTIVES Edited by Larissa Swedell and Steven R. Leigh PRIMATE ORIGINS: ADAPTATIONS AND EVOLUTION Edited by Matthew J. Ravosa and Marian Dagosto RINGTAILED LEMUR BIOLOGY: LEMUR CATTA IN MADAGASCAR Edited by Alison Jolly, Robert W. Sussman, Naoki Koyama and Hantanirina Rasamimanana RINGTAILED LEMUR BIOLOGY

Lemur Catta in Madagascar

Edited by Alison Jolly University of Sussex Brighton, United Kingdom Robert W. Sussman Washington University St. Louis, Missouri, USA Naoki Koyama Kyoto University Kyoto, Japan Hantanirina Rasamimanana University of Antananarivo Antananarivo, Madagascar Alison Jolly Robert W. Sussman Department of Biology and Department of Anthropology Environmental Sciences Washington University University of Sussex St. Louis, Missouri 63130-4899 Lewes BN7 1HX, Brighton USA UK [email protected] [email protected]

Naoki Koyama Hantanirina Rasamimanana Center for African Area Studies École Normale Supérieure Kyoto University University of Antananarivo Kyoto 606-8501 BP 881 JAPAN Antananarivo 101 [email protected] MADAGASCAR [email protected]

Library of Congress Control Number: 2006921354

ISBN 10: 0-387-32669-3 ISBN 13: 978-0387-32669-6

Printed on acid-free paper.

© 2006 Springer Science+Business Media, LLC All rights reserved. This work may not be translated or copied in whole or in part without the written permission of the publisher (Springer Science+Business Media, LLC, 233 Spring Street, New York, NY 10013, USA), except for brief excerpts in connection with reviews or scholarly analysis. Use in connection with any form of information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed is forbidden. The use in this publication of trade names, trademarks, service marks, and similar terms, even if they are not identified as such, is not to be taken as an expression of opinion as to whether or not they are subject to proprietary rights. While the advice and information in this book are believed to be true and accurate at the date of going to press, neither the authors nor the editors nor the publisher can accept any legal responsibility for any errors or omissions that may be made. The publisher makes no warranty, express or implied, with respect to the material contained herein.

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987654321 springer.com Preface

This book is a truly international collaboration, with editors based on four conti- nents and first authors from Canada, France, Japan, Madagascar, the United Kingdom, and the United States. Clearly, there is something attractive about studying Lemur catta, the ringtailed lemur. Perhaps it is the lemurs themselves! Why study ringtailed lemurs? Because lemurs are a separate radiation of primates from the monkeys, apes, and humans. Because ringtails live in the largest social groups of any known lemur and therefore offer the closest comparison with other social primates, including ourselves. And also because ringtails have become the flagship species of Madagascar. Some 70 species or subspecies of lemurs inhabit Madagascar. Each kind has its own fascinating story, but ringtails are the ones that everyone thinks they know. That black-and-white tail adorns tourist brochures and school notebooks and banknotes. All the same, after 40 years of field study, we don’t know nearly enough. In this book, we make a first estimate on how many might be alive today, but we do not know how many ringtailed lemurs and how many southern forests will survive. This book explores part of what we do know. Its four sections are (I) Distribution: Ringtailed Lemurs in Madagascar, (II) Ringtails and Their Forests: Feeding and Ranging Behavior, (III) Social Behavior Within and Between Troops, and finally (IV) Health and Disease. Of course, all these issues are inter- related. We would like to point out some cross-cutting themes that emerge from the chapters if read as a whole. The first is that the southern area of Madagascar, where the ringtails live, spans a huge variety of habitats and a huge variation of year-to-year fluctuations in climate. The range of ringtails lies mainly in very dry spiny forests and marginal scrub, but they also flourish in rich, tamarind-dominated gallery forests, in the fortress canyons of the Isalo, and even above the tree-line on the Andringitra Massif (Goodman et al. and Sussman et al. on range). Beza Mahafaly Reserve and Berenty Reserve, the only two long-term study sites, Both lie in gallery forest and thus represent the homes of lemur plutocrats rather than more widespread and more challenging habitats (Sussman et al. on Beza, Jolly et al. on Berenty). Even within such favored areas though, the effect of recurrent drought can be catastrophic. It shapes everything Ð from population size to life history to

v vi Preface microevolution (Jolly et al. on territoriality as bet hedging; Cuozzo and Sauther on tooth microevolution). Furthermore, the small patches of gallery forest have always been discontinuous, and they have shifted in space over a timescale of decades or centuries even before people began to clear them (Blumenfeld-Jones et al. on tamarind recruitment). Thus, any overview of the species needs the widest possible spread in space and time, because no one year, and not even any one forest, can be called “typical.” In fact, ringtailed lemurs as a species are adapted to difference and challenge. This is one reason why they are so well known. Zoos love to exhibit them, not only as striking animals but also because they are semiterrestrial, diurnal, at home in discontinuous habitat, and individually as tough as old boots. The second theme is the importance of tamarind trees, Tamarindus indica. This keystone resource provides food year round, whether green pods in the dry, cold winter season when females are gestating, ripe fruit as the young are born and lac- tation begins, or fruit and leaves when the young are weaned. Years when the fruit fails are disastrous for the lemurs. Long-term patterns of tamarind growth and regeneration determine lemur use of the richest of their forest habitats If the ringtails’ access to the tamarinds is limited by competing brown lemurs, this is also likely to have a major impact on their populations and distribution. (Simmen et al., plant food species; Blumenfeld-Jones, tamarind recruitment; Koyama et al., tamarinds and home range; Mertl-Millhollen et al., tamarind quality; Simmen et al., taste thresholds; Cuozzo and Sauther, tooth microevolution; Pinkus et al., brown lemur competition). The third theme is the extreme role played by females in troop coherence, troop rivalry, and resource defense. Female dominance over males does not reflect dif- ferential energy expenditure (Rasamimanana et al., energetic strategy). However, it is clear that intertroop female resource defense is crucial in gallery forest (Pride et al., group size and defense). Within a troop, females vie directly for status (Pereira, agonistic power). Status in turn is fundamental to continued troop membership. Subordinates exiled by targeted aggression may roam as all-female nomadic groups for many months before they succeed in establising defended ranges (Ichino et al., social changes). Even then the ranges are usually inferior to those held by former dominants: inequality may be perpetuated over generations (Jolly et al., territory as bet hedging). Immigrant males as postulants for troop membership seem secondary to the troop structure, though crucial for the mixing of genes (Gould et al., male migration). But males are still an unsolved riddle: why do such combative, polygamous animals not evolve dominance over females? A fourth theme is the role of health and disease, particularly in human-altered habitats. At Berenty Reserve, the lemurs have adopted introduced species as foods, which have benefited them, allowing massive population growth (Soma et al., introduced trees; Simmen et al., food plants). However, Leucaena, a legu- minous tree originating from Central America that has been planted worldwide by foresters for fuel wood and livestock forage, actually poisons some Berenty lemurs (Crawford et al., bald lemur syndrome; Soma et al., introduced trees) Even Preface vii in the more natural forest of Beza Mahafaly, lemurs put on weight when they have access to campsite foods, though they pay a price in tooth decay (Sauther et al., health and disease). Tooth wear reflects interactions between the lemurs, their society, the impact of drought, and their keystone tamarind resources (Cuozzo and Sauther, tooth microevolution). The interaction between health and habitat change will be an ever-increasing concern of the emerging field of conservation medicine. Finally, there is the overarching question of ringtailed lemur conservation. Sussman et al. estimate that between 1985 and 2000, 9.5% of forest habitat suitable for ringtailed lemurs has been lost. In this period, the population may have fallen from a possible 930,000 ringtailed lemurs down to 750,000, a 20% reduc- tion, even under the unlikely assumption that all suitable habitat is occupied by lemurs. Add to this the pressures from natural changes (Blumenfeld-Jones et al., Koyama et al., Cuozzo et al., Jolly et al.) and the pressures brought by even well- meaning human intervention, let alone hunting and forest fragmentation (Sauther et al.; Crawford et al.; Pinkus et al.), many forests that look suitable to an orbit- ing satellite will not in fact hold any lemurs. Still, the species is both widespread and adaptable, classified as vulnerable, not endangered. The future of ringtailed lemurs is not a story of their own biology. It is a story of how people value their habitat and their survival. Long may they remain a flagship species for Madagascar! The Editors Contents

Contributors...... xiii

PART I: DISTRIBUTION: RINGTAILED LEMURS IN MADAGASCAR ...... 1

1. The Distribution and Biogeography of the Ringtailed Lemur (Lemur catta) in Madagascar ...... 3 Steven M. Goodman, Soava V. Rakotoarisoa, and Lucienne Wilmé

2. A Preliminary Estimate of Lemur catta Population Density Using Satellite Imagery...... 16 Robert W. Sussman, Sean Sweeney, Glen M. Green, Ingrid Porton, O.L. Andrianasolondraibe, and Joelisoa Ratsirarson

3. Berenty Reserve: A Research Site in Southern Madagascar ...... 32 Alison Jolly, Naoki Koyama, Hantanirina Rasamimanana, Helen Crowley, and George Williams

4. Beza Mahafaly Special Reserve: A Research Site in Southwestern Madagascar ...... 43 Robert W. Sussman and Joelisoa Ratsirarson

PART II: RINGTAILS AND THEIR FORESTS: FEEDING AND RANGING ...... 53

5. Plant Species Fed on by Lemur catta in Gallery Forests of the Southern Domain of Madagascar...... 55 Bruno Simmen, Michelle L. Sauther, Takayo Soma, Hantanirina Rasamimanana, Robert. W. Sussman, Alison Jolly, Laurent Tarnaud, and Annette Hladik

ix x Contents

6. Tamarind Recruitment and Long-Term Stability in the Gallery Forest at Berenty, Madagascar ...... 69 Kathryn Blumenfeld-Jones, Tahirihasina M. Randriamboavonjy, George Williams, Anne S. Mertl-Millhollen, Susan Pinkus, and Hantanirina Rasamimanana

7. Home Ranges of Ringtailed Lemur Troops and the Density of Large Trees at Berenty Reserve, Madagascar. . 86 Naoki Koyama, Takayo Soma, Shinichiro Ichino, and Y. Takahata

8. The Influence of Tamarind Tree Quality and Quantity on Lemur catta Behavior ...... 102 Anne S. Mertl-Millhollen, Hajarimanitra Rambeloarivony, Wendy Miles, Veronica A. Kaiser, Lisa Gray, Loretta T. Dorn, George Williams, and Hantanirina Rasamimanana

9. Feeding Competition Between Introduced Eulemur fulvus and Native Lemur catta During the Birth Season at Berenty Reserve, Southern Madagascar ...... 119 Susan Pinkus, James N.M. Smith, and Alison Jolly

10. Tradition and Novelty: Lemur catta Feeding Strategy on Introduced Tree Species at Berenty Reserve ...... 141 Takayo Soma

11. Diet Quality and Taste Perception of Plant Secondary Metabolites by Lemur catta...... 160 B. Simmen, S. Peronny, M. Jeanson, A. Hladik, and A. Marez

PART III: SOCIAL BEHAVIOR WITHIN AND BETWEEN TROOPS ...... 185

12. Territory as Bet-hedging: Lemur catta in a Rich Forest and an Erratic Climate ...... 187 Alison Jolly, Hantanirina Rasamimanana, Marisa Braun, Tracy Dubovick, Christopher Mills, and George Williams

13. Resource Defense in Lemur catta: The Importance of Group Size ...... 208 R. Ethan Pride, Dina Felantsoa, Tahiry Randriamboavonjy, and Randriambelona Contents xi

14. Social Changes in a Wild Population of Ringtailed Lemurs (Lemur catta) at Berenty, Madagascar ...... 233 Shinichiro Ichino and Naoki Koyama

15. Obsession with Agonistic Power ...... 245 Michael. E. Pereira

16. Male and Female Ringtailed Lemurs’ Energetic Strategy Does Not Explain Female Dominance ...... 271 Hantanirina Rasamimanana, Vonjy N. Andrianome, Hajarimanitra Rambeloarivony, and Patrick Pasquet

17. Male Sociality and Integration During the Dispersal Process in Lemur catta: A Case Study ...... 296 Lisa Gould

PART IV: HEALTH AND DISEASE ...... 311

18. Patterns of Health, Disease, and Behavior Among Wild Ringtailed Lemurs, Lemur catta: Effects of Habitat and Sex ...... 313 Michelle L. Sauther, Krista D. Fish, Frank P. Cuozzo, David S. Miller, Mandala Hunter-Ishikawa, and Heather Culbertson

19. Bald Lemur Syndrome and the Miracle Tree: Alopecia Associated with Leucaena leucocephala at Berenty Reserve, Madagascar ...... 332 Graham C. Crawford, Louis-Expert Andriafaneva, Kathryn Blumenfeld-Jones, Gary Calaba, Linda Clarke, Lisa Gray, Shinichiro Ichino, Alison Jolly, Naoki Koyama, Anne Mertl-Millhollen, Susan Ostpak, R. Ethan Pride, Hantanirina Rasamimanana, Bruno Simmen, Takayo Soma, Laurent Tarnaud, Alison Tew, and George Williams

20. Temporal Change in Tooth Size Among Ringtailed Lemurs (Lemur catta) at the Beza Mahafaly Special Reserve, Madagascar: Effects of an Environmental Fluctuation...... 343 Frank P. Cuozzo and Michelle L. Sauther

Index...... 367 Contributors

Andriafaneva, L.-E. c/o Berenty Reserve, BP 54, Tolagnaro (Fort Dauphin), Madagascar Andrianasolondraibé, O.L., Département de Paléontologie, Anthropologie et Biologie, Université d’Antananarivo (101), Madagascar, harivony@ wanadoo.mg Andrianome, V.N., École Normale Supérieur, University of Antananarivo, BP 881, Antananarivo, Madagascar, [email protected] Blumenfeld-Jones, K. Dept. of Anthropology, Arizona State University, Tempe, Arizona, [email protected], [email protected] Braun, M. Graduate School of Medicine, George Washington University, Washington DC 20052 USA, [email protected] Calaba, G. 4141 Laddington Ct., Portland, OR 97232, USA, calaba@ ipns.com Clarke, L. San Francisco Zoological Society, San Francisco CA 94132-1098, USA Crawford, G.C. San Francisco Zoological Society, San Francisco CA 94132- 1098, USA, [email protected] Crowley, H. Wildlife Conservation Society, BP 8500, Antananarivo, Madagascar, [email protected] Culbertson, H. College of Veterinary Medicine, Cornell University, Ithaca, NY 14850, USA, [email protected] Cuozzo, F. Department of Anthropology, University of North Dakota, Grand Forks, ND 58202, USA, [email protected] Dorn, L.T. Department of Chemistry, Fort Hays State University, Hays, KS, USA, [email protected] Dubovick, T. School of Veterinary Medicine, University of Pennsylvania, Philadelphia PA 19104, USA, [email protected] Felantsoa, D. Dept. of Biology, Ècole Normale Superieur, University of Antananarivo, BP 881 Madagascar, [email protected] Fish, K. University of Colorado Boulder, Department of Anthropology, Box 233, Boulder, CO 80309-0233, USA, [email protected]

xiii xiv Contributors

Goodman, S.M. Field Museum of Natural History, Chicago, Illinois, 60605, USA, [email protected], WWF, B.P.738, Antananarivo (101), Madagascar, [email protected], Gould, L. Department of Anthropology, University of Victoria, Victoria BC Canada, [email protected] Gray, L. Joint Information Systems Committee, University of Bristol, Bristol, UK, [email protected] Green, G.M. Center for the Study of Institutions, Population and Environmental Change (CIPEC) Indiana University, Bloomington, IN 47408, USA, [email protected] Hladik, A. Eco-Anthropologie et Ethnobotanique, Muséum National d’Histoire Naturelle/CNRS, 4 avenue du Petit-Château, 91800 Brunoy, France, [email protected] Hunter-Ishikawa, M. College of Veterinary Medicine and Biomedical Sciences, Colorado State University, Fort Collins CO 80523-1601, USA, [email protected] Ichino, S. Laboratory of Human Evolution Studies, Graduate School of Science, Kyoto University Kitashirakawaoiwake-cho, Sakyo-ku, Kyoto 606-8502 Japan, [email protected] Jeanson, M. Eco-Anthropologie et Ethnobotanique, Muséum National d’Histoire Naturelle/CNRS, 91800 Brunoy, France, marcjeanson@ yahoo.fr Jolly, A. Department of Biology and Environmental Science, University of Sussex, Brighton BN1 9QG, UK, [email protected] Kaiser, V.A. Department of Biology and Environmental Science, University of Sussex, Brighton BN1 9QG, UK, [email protected] Koyama, N. Center for African Area Studies, Kyoto University, Kyoto 606- 8501, Japan, [email protected] Marez, A. IUT, Département Génie Biologique, Université Paris XII, Avenue du Général de Gaulle, 94010 Créteil, France, [email protected] Mertl-Millhollen, A.S. University of Oregon, Dept. of Anthropology, Eugene, OR 97403 USA, [email protected] Miles, W. Oxford University Center for the Environment, Oxford University, Oxford OX1 2JD, UK, [email protected] Miller, D.S. Animal Population Health Institute, College of Veterinary Medicine and Biological Sciences, Colorado State University, Fort Collins CO 80523, USA, [email protected] Mills, C. 645 El Dorado Ave # 308, Oakland CA 94611, USA, chrisnmills@ yahoo.com Ostpak, S. San Francisco Zoological Society, San Francisco CA 94132-1098, USA, [email protected] Pasquet, P. CNRS, Muséum de l’Histoire Naturelle, 75231 Paris, Cedex 05, France, [email protected] Pereira, M.E. The Latin School of Chicago, 59 West North Boulevard, Chicago, IL 60610-1492, [email protected] Contributors xv

Peronny, S. Eco-Anthropologie et Ethnobotanique, Muséum National d’Histoire Naturelle/CNRS, 4 avenue du Petit-Château, 91800 Brunoy, France, [email protected] Pinkus, S. Department of Ecology, University of British Columbia, Vancouver, Canada, [email protected] Porton, I. St. Louis Zoo, 1 Government Drive, St. Louis, Missouri, 63110- 1395, USA, [email protected] Pride, R.E. CAS Biology, Boston University, 5 Cummington St. Boston MA 02215, USA, [email protected] Rakotaoarisoa, S.V. Programme Alimentaire Mondial (PAM), BP 1348, Antananarivo (101), Madagascar, [email protected] Rambeloarivony, H. Dept. of Biology, Ècole Normale Superieur, University of Antananarivo, BP 881, Madagascar, [email protected] Randriambelona, R. Parc Ivoloina, Madagascar Fauna Group, BP 442, Toamasina (501) Madagascar, [email protected] Randriamboavonjy, T.M. Dept. of Biology, Ècole Normale Superieur, University of Antananarivo, BP 881 Madagascar, tahiry@vodka orange.com Rasamimanana, H. École Normale Supérieur, Université d’Antananarivo, BP 881, Antananarivo 101, Madagascar, [email protected] Ratsirarson, J. Départment des Eaux et Forêts de l’Ecole Supérieur des Sciences Agronomiques, Université d’Antananarivo (101) Madagascar, [email protected] Sauther, M.L. University of Colorado Boulder, Department of Anthropology, Hale Building, Box 233, Boulder, CO 80309-0233, USA, michelle. [email protected] Simmen, B. Eco-Anthropologie et Ethnobotanique, Muséum National d’Histoire Naturelle/CNRS, 4 avenue du Petit-Château, 91800 Brunoy, France, [email protected] Smith, J.N.M. Department of Ecology, University of British Columbia, Vancouver, Canada Soma, T. Center for African Area Studies, Kyoto University, 46 Shimoadachicho, Yoshida, Sakyo-ku, Kyoto 606-8501, Japan, soma@ jambo. africa.kyoto-u.ac.jp Sussman, R.W. Department of Anthropology, Washington University, Campus Box 114, One Brookings Drive, St. Louis, Missouri 63130- 4899 USA, [email protected] Sweeney, S. Center for the Study of Institutions, Population and Environmental Change (CIPEC) Indiana University, 408 N. Indiana Ave., Bloomington, IN 47408, USA, [email protected] Takahata, Y. Kwansei Gakuin University, Sanda, 669-1337, Japan, z96014 @ksc.kwansei.ac.jp Tarnaud, L. Eco-Anthropologie et Ethnobotanique, Muséum d’Histoire Naturelle/CNRS, 4 avenue du Petit-Château, 91800 Brunoy, France, [email protected] xvi Contributors

Tew, A. Department of Anthropology, Oxford Brookes University, Oxford, UK, [email protected] Williams, G. 44 Alan Road, Santa Barbara, CA 93109, USA, gww@ silcom.com Wilmé, L. Missouri Botanical Garden, BP 3391, Antananarivo (101) Madagascar, [email protected]